Pulmonologists' Perspectives on and Access to Palliative Care for Patients With Idiopathic Pulmonary Fibrosis in South Carolina

Background: Idiopathic pulmonary fibrosis (IPF) is a serious illness with an unpredictable disease course and survival rates comparable with some cancers. Patients with IPF suffer considerable symptom burden, declining quality of life, and high health care resource utilization. Patients and caregivers report many unmet needs, including a desire for more education regarding diagnosis and assistance with navigating disease trajectory. Compelling evidence suggests that palliative care (PC) provides an extra layer of support for patients with serious illness. Research Question: The purpose of this survey was to gain perspectives regarding PC for patients with IPF by board-certified pulmonologists in South Carolina (SC). Study Design and Methods: A 24-item survey was adapted (with permission) from the Pulmonary Fibrosis Foundation PC Survey instrument. Data were analyzed and results are presented. Results: Pulmonologists (n = 32, 44%) completed the survey; 97% practice in urbanized settings. The majority agreed that PC and hospice do not provide the same service. There were varying views about comfort in discussing prognosis, disease trajectory, and addressing advance directives. Options for ambulatory and inpatient PC are limited and early PC referral does not occur. None reported initiating a PC referral at time of initial IPF diagnosis. Interpretation: Pulmonologists in SC who participated in this survey are aware of the principles of PC in providing comprehensive care to patients with IPF and have limited options for PC referral. PC educational materials provided early in the diagnosis can help facilitate and guide end-of-life planning and discussions. Minimal resources exist for patients in underserved communities.


Introduction
Idiopathic pulmonary fibrosis (IPF), a progressive lung disease of aging, affects *250,000 people in the United States, with 50,000 new cases diagnosed each year. 1 IPF is a serious illness with an unpredictable disease course 2 with survival rates comparable with some aggressive cancers. 3Despite the advances that slow disease progression, most patients with IPF succumb to their disease or require lung transplant within five years of diagnosis. 4atients newly diagnosed with IPF, and their caregivers must quickly adapt to lives dominated by a chronic progressive disease.For the patient, this is associated with declining physical function, constraints of supplemental oxygen, social isolation, impaired quality of life, shortened lifespan, and high health care resource utilization. 5A diagnosis of IPF is burdensome for the caregiver as well, who may feel an overwhelming sense of fear of the unknown and often, due to age, has their own comorbidities to manage. 6Patients and their caregivers report many unmet needs, including a desire for more education regarding their diagnosis and assistance with navigating disease trajectory. 7,8nternational and national guidelines recommend that palliative care (PC) be offered to patients who are diagnosed with serious illnesses, including IPF. 2,[9][10][11] Compelling evidence suggests that PC provides an extra layer of support while patients with serious illness receive nonpharmacological and pharmacological therapies. 12][17][18][19] Social determinants of health (SDOH) further complicate access to care and neighborhood disadvantage negatively impacts mortality. 20Disparities related to health care access, particularly for those residing in medically underserved areas and/or rural communities, create barriers to health equity. 21Located on southeastern U.S. coast, South Carolina (SC) has a population of 5,282,634 residents: White 68.8%,Black 26.7%, and Hispanic 6.4%, and is predominantly rural with 40 of its 46 counties defined as rural by the U.S. Census (Fig. 1). 22ith an estimated population of 170 residents per sq.mile, more than 95% of the population live in a Primary Care Health Professional Shortage Area and 17.6% live in poverty.It is difficult to determine the exact incidence and prevalence of IPF in SC, but chronic lower respiratory disease is the fifth leading cause of death 23 in the state at a rate of 43.6 deaths per 100,000, ranking SC as the 11th highest state in the United States.The most recent data for the state of SC published in December 2019 suggest that, although it is difficult to quantify the ongoing burden of serious illness in the state, of the South Carolinians who died in 2018 an estimated 53.8% would have been eligible for PC but did not receive it. 24n 2021, the Pulmonary Fibrosis Foundation (PFF) conducted a survey 25 among 128 health care providers across 68 PFF Care Center Network sites 26 in the United States about current perspectives on PC for pulmonary fibrosis (PF) patients and barriers to PC for this patient population.In conclusion, they found most providers utilize PC, but there is lack of established optimal timing for PC referral. 25Furthermore, this study was conducted in specialty PFF Centers and thus may not represent the perspectives of community practicing pulmonary physicians.
The purpose of this survey was to gain pulmonologists' perspectives on and access to PC for patients with IPF and their caregivers in SC, a rural state with significant health care disparities. 27

Setting and participants
This study was conducted among board-certified pulmonologists who practice in SC and care for patients with IPF.The current workforce of pulmonologists in SC lists 72 pulmonologists with 71,510 people per physician, ranking 36th in the United States for active pulmonologists per 100,000 population. 28

Survey instrument
The 24-item survey was adapted (with permission) from the PFF PC Survey 25 instrument and converted by the researchers into a Research Electronic Data Capture (REDCap) survey for online dissemination.

Data collection and management
This study used REDCap hosted on secure institutional servers to disseminate the survey, collect, and manage data.All pulmonologists in SC 28 were sent a REDCAP survey invitation link through e-mail using features that prevented linking pulmonologists to their responses.Pulmonologists received four-monthly automated system reminders to complete the survey.Data were collected from June to September 2022.

Statistical analysis
Data were analyzed using Microsoft Excel 16.6.Results are presented using basic descriptives (frequencies and percentages) to summarize findings.The frequencies of missing returned data are presented in the data tables; however, they are excluded from the final analysis.

Ethical considerations
Per Medical University of South Carolina (MUSC) Institutional Review Board (IRB), this project was not subject to IRB review or approval.All participants were informed of the voluntary nature of survey completion and could refuse to respond to any question or stop participation at any time.Given the same sample size of registered in SC and the potential for the identification of individuals and/or respective employers based on responses, participant's race and ethnicity data are not presented, and practice zip code data has been aggregated in reporting to protect their privacy and confidentiality.Study compensation was not provided to participants for survey completion.

Results
Seventy-two board-certified pulmonologists practice in SC; 44% (32/72) completed the survey.The majority (75%) of these respondents reported more than five years of experience in providing care to IPF patients (Table 1) and *97% practice in cities (>2500 people) and 3% in rural areas (<2500 people) of SC, respectively (Fig. 1).Most could differentiate PC and hospice.Just more than one third of respondents were very comfortable discussing prognosis, disease trajectory, and readiness for PC.
Less than one third of the respondents strongly agreed that they addressed advance directives with patients.The majority evaluated symptoms quarterly, however, did not report use of a standardized instrument to assess symptom burden.Less than one quarter of respondents strongly agreed that they used PC with varied results on availability of PC resources and timing of referral.Lastly, the majority reported that handouts describing the disease and PC options for IPF patients and caregivers would be helpful (Table 2).

Discussion
The purpose of this survey was to gain pulmonologists' perspectives on and access to PC for patients with IPF and caregivers in SC, a rural state with significant  health care disparities. 27Survey findings reveal that these pulmonologists had knowledge that PC and offered different services.Comfort in communication practices differed for these respondents.Particularly concerning in the results are the relatively small proportions (*30%) of practicing pulmonologists that reported strongly agreeing with their comfort level discussing prognosis and referral to PC with their IPF patients.
If a patient's pulmonologist does not feel proficient in having these difficult conversations, the question begs will this conversation occur and who will have it.While pulmonologists endorsed querying patient's symptom burden and quality of life, very few used structured tools to accomplish this goal.This is concerning that respondents may not be systematically evaluating patient symptom burden, including anxiety and depression, and related treatment options.The majority had access to some level of PC, but referral to PC was reported not to occur early in the disease course for patients with IPF.Approximately one-half of pulmonologists (47%) refer to PC when the patient is hospitalized.
These findings support past work about unmet patient needs 7,8 and delayed referral for PC. 19,29,30here are several reasons why patients with IPF are not referred to PC or referred late in the disease course.These include limited time during the office visit to have this serious illness discussion, many providers are uncomfortable with PC and fear that such discussions will diminish hope, and limited PC resources. 31he serious nature of IPF, compounded by the unpredictable disease course, mandates that serious illness communication should occur early after diagnosis to promote symptom management and identify patient's  wishes as they address end of life (EOL). 32Patients whose prioritized health care goals are understood by their clinicians likely to be better positioned to receive goal-concordant care, defined as ''medical care that aligns with the patients' values, goals, and life priorities. 33,34PC provides this extra layer of support while patients with serious illness receive nonpharmacological and pharmacological therapies throughout their disease course. 12ullivan et al. propose a model for collaborative PC in serious respiratory illness with a joint collaboration between pulmonologists and primary and specialty PC providers early in the disease. 35Although our study did not query pulmonologists' perception of telehealth as a tool to increase access to PC, this has been shown to be a feasible and acceptable approach and can be facilitated through telehealth delivery to patients and caregivers earlier in the disease course, including those in underserved and/or rural communities. 36Remote monitoring of patients enrolled in PC through telehealth has been shown to be acceptable and feasible. 37ddressing SDOH that compound barriers in access to PC for patients with IPF and caregivers is of high importance.Similar to many states, SC is largely rural, where many patients travel a significant distance to receive specialty care to confirm diagnosis and treatment plan.In addition, many of these patients lack reliable transportation compounding SDOH.These patients then frequently return to remote areas that lack resources, including partners in care, thus leading to health care deprivation and social isolation.The most deprived counties cluster in rural parts of SC, whereas the more affluent counties cluster in the more urban parts of the state.It is important to note that there are urban areas in SC that are underserved. 22In previous study, we found that patients with IPF living in neighborhoods with greater disadvantage experienced higher mortality. 20

Limitations
This survey was conducted among board-certified pulmonologists in SC and may not be reflective of the care patients with IPF receive in PFF Centers.Although we adapted and disseminated a survey instrument that had previously been devised by an expert panel and used to explore IPF provider's perceptions on a national level, the instrument has not yet been validated.Owing to the small sample size, the observed 44% (32/72) response rate may limit the generalizability of our findings.
This survey would benefit from replication in other states with similar rural geography to look for similarities or differences in practice.In addition, although this survey assessed pulmonologist's perceptions of and access regarding PC in our state, there is no patient-level data to determine what happens from the patient/caregiver voice.As mentioned earlier, of the South Carolinians who died in 2018 an estimated 53.8% would have been eligible for PC but did not receive it.This report does not break down by disease category or practitioner type. 24terpretation Pulmonologists in SC who participated in this survey are aware of the principles of PC in providing comprehensive care to patients with IPF.Symptom management was viewed to be important but widespread use of standardized tools to measure symptom burden is uncommon.This is understandable in a busy clinical practice where the focus is on the physician/patient interaction but raises concerns about unmet symptom assessment and management needs.Educational resources are needed to increase the pulmonologists' comfort in facilitating conversations around PC as well as help explain the disease trajectory early in diagnosis, and to facilitate EOL care planning (e.g., advance directives).
With limited options for PC referrals, we endorse use of other avenues for early delivery of PC including national PC resources where providers and patients can access information about PC, for example, Get.PC .com:https://getpalliativecare.org/ 38 and PFF PC Position Statements for Providers and Patients. 39,40ke-Home Points Communication of serious illness is critical for patients diagnosed with IPF and caregiver(s).
Practicing pulmonologists should seek proficiency in having these serious illness discussions regarding prognosis and referral to PC for IPF patients.
SC workforce of pulmonologists ranks 36th in the nation; this workforce shortage may contribute to delay in PC discussion.
PC resources are available to guide patients and caregivers to independently seek out PC.
Telehealth delivery of PC and nurse-led programs can address the SDOH and access to PC.

FIG. 1 .
FIG. 1. Geographic distribution of returned surveys by pulmonologists' practice zip code and state level (SC) 2018 U.S. Census population estimates.SC, South Carolina.

Table 2 .
South Carolina Pulmonologist's Survey Results